Endocrine Disrupters and Bald Eagles: A Response

By: Robert W. Risebrough

I should like to thank the editor of the Endangered Species UPDATE for
the opportunity to comment on the article "Endocrine Disruption: Hidden
Threats to Wildlife" by Michael Smolen and Theo Colborn of the World
Wildlife Fund in the September/October 1997 issue. The conclusion of this
article is that a very wide range of wildlife species is now threatened
by a diverse assortment of synthetic chemicals in the environment. Their
effects are initially hidden but in the longer term reproductive abnormalities
and disruptions in other essential life processes result from the "stealth
damage caused by interference with endogenous messengers" (Smolen and
Colborn 1997:10).

Thirty years ago, this statement would have been at least partly true,
with an important qualification: the effects at that time were hardly hidden.
Peregrine falcons (Falco peregrinus) had become extinct as a breeding
species over half of the country. Bald eagle (Haliaeetus leucocephalus)
populations were rapidly declining. The state bird of Louisiana, the brown
pelican (Pelecanus occidentalis), once numerous, was no longer breeding
in the delta of the Mississippi. Everywhere, fish-eating birds were in trouble.
A process of extinction, without precedent in evolutionary history, was
threatening the integrity of ecosystems.

In 1968, six years after Silent Spring (Carson 1962), there was as yet
little control over the application of vast quantities of the chlorinated
hydrocarbon pesticides then still in widespread use; polychlorinated biphenyls
(PCBs), not yet known to be environmental contaminants of greater significance
than the biocides, could be purchased in railway-car amounts for incorporation
into a diversity of industrial products.

In that year, the spraying programs to "eradicate" Dutch elm
disease in Milwaukee were continuing to kill countless numbers of songbirds,
prompting a group of citizens to petition the Wisconsin Department of Natural
Resources. The Hearing Examiner ruled that he had no legal authority to
stop the spraying program, but pointed out that a law on the Wisconsin books
prohibited the use in that state of any substance that, as a consequence
of its use, entered the waters of the state and caused harm to wildlife.
The stage was set for a confrontation between the environmentalists, represented
by the Environmental Defense Fund, and the pesticide industry. In less than
a decade the uses of the major chlorinated hydrocarbon pesticides had ended
in the USA and most of the other industrialized countries; PCBs were no
longer manufactured in North America and a process, inevitably imperfect,
to prevent future 'PCBs' (chemicals that are persistent, mobile in the environment,
with unpredictable biological activity) was implemented by the Toxic Substances
Control Act.

Recovery of the wildlife populations affected by these contaminants,
although dramatic for peregrine falcons and most populations of the bald
eagle, has not happened overnight, and is not yet complete. Environmental
contamination by the persistent biocides, although declining, continues
to affect populations of sensitive species. How then are the remnant 'old'
effects, those caused by the chemicals whose uses ended a generation or
more ago, to be distinguished from the 'new' "hidden threats"
that are the subject of the article by Smolen and Colborn

The example of a 'new' threat that is discussed in greatest detail is
the continuing lower productivity of bald eagles nesting on the shores of
the Great Lakes, even though "Eggshell thinning and outright mortality
are no longer visible" (Smolen and Colborn 1997:6). The balance of
the scientific evidence, however, indicates that this is a remnant 'old'
effect; in part, the evidence comes from a population of bald eagles reintroduced
to Santa Catalina Island in southern California that continues to suffer
from severe effects of contamination by DDE, the environmental derivative
of DDT that has been responsible for all, or almost all, of the eggshell
thinning documented since 1946. The argument derives from multiple sources.

1) The bald eagle was the first species for which an effect at the population
level induced by an environmental contaminant was documented. A retired
Canadian banker, Charles Broley from Winnipeg, began to band nestling bald
eagles in Florida in 1939. By 1946, he had reached 150 young eagles a year.
But in 1947 the number of young eagles dropped sharply and continued to
drop in the following years (Broley 1958).

2) Beginning abruptly in 1947, the weights of eggshells and the eggshell
thickness of Florida bald eagles dropped by 15-19 % (Hickey and Anderson
1968; Anderson and Hickey 1972), coinciding with the sudden depression of
productivity observed by Broley.

3) The eggshell weight and the shell thicknesses of other species of
raptorial birds also declined abruptly in 1947 in other areas of North America
(Hickey and Anderson 1968; Anderson and Hickey 1972) and in Britain (Ratcliffe
1967).

4) Like the brown pelican and the prairie falcon (Falco mexicanus),
the bald eagle is very sensitive to DDE. Reproduction invariably fails whenever
concentrations in the eggs exceed a few parts per million, whether the relationship
is expressed logarithmically with a pronounced effect even at the lowest
levels of DDE (Wiemeyer et al. 1984, 1993) or by a model that assumes a
minimum effect at the lowest levels with a sharp decrease above a threshold
(Nisbet 1989).

5) Unlike species such as the brown pelican, whose eggs break above a
critical level of thinning thereby accounting for a major portion if not
all of the reproductive failures, productivity of bald eagles is, unexpectedly,
not related to shell thinning, but is nevertheless strongly related to DDE
concentrations (Nisbet 1989). This DDE effect on reproduction is therefore
distinct from eggshell thinning.

6) Bald eagles disappeared from the southern California islands during
the 1950s (Kiff 1980) when wastes from a DDT factory in Los Angeles, containing
many tons of DDT, were taken in barges to sea throughout the 1950s for offshore
dumping. Following recovery of the brown pelicans in the mid-1970s, they
were reintroduced to Santa Catalina Island beginning in 1980 by David Garcelon
of the Institute for Wildlife Studies. The first egg appeared in 1987, but
it broke shortly after being laid. Shell fragments with portions of the
yolk were retrieved for analysis in my laboratory. The California Bald Eagle
Working Team was to meet the following week on Santa Catalina Island; there
was a certain urgency to report both the contaminant levels and the degree
of shell thinning. On a lipid basis DDE concentrations were five times higher
than the threshold level of reproduction effects. On the day of the meeting,
Sam Sumida of the Western Foundation of Vertebrate Zoology, measured shell
thickness. It was almost normal. We had no explanation why the egg had broken.
In 1988 a second female produced an egg which also broke in the nest almost
immediately after being laid. Its shell thickness was also almost normal,
and the DDE levels were high (Garcelon et al. 1989; Jenkins et al. 1994).

7) Thereafter eggs have been collected as soon as possible for artificial
incubation, initially at the Santa Cruz Predatory Bird Group and currently
at the San Francisco Zoo. Only if exhaustive measures are taken to control
the rate of water loss from the egg is the embryo able to survive. David
Garcelon reports that one of this year's breeding males was hatched in 1992
from a deformed egg artificially incubated by the Santa Cruz Predatory Bird
Group in 1992 while his parents incubated a dummy egg on Santa Catalina
Island. Like his parents before him, he and his mate incubated dummy eggs
after their own deformed eggs were removed. This year's chicks, however,
died at the pipping stage, despite all the efforts of the zoo personnel
to nurse them through the hatching process (D.K. Garcelon, personal communication).

8) Scanning electron microscopy detected small areas of gross structural
abnormalities of the eggshell (Figures 1 and 2), associated with gross changes
of the organic crystallization sites on the eggshell membrane (Bland 1990;
Risebrough 1993). The rapid rate of water loss and the embryonic deaths
were thereby explained; these structural abnormalities could also have produced
a weakening of the eggshell that resulted in breakage in the absence of
any significant thinning.

9) There are no DDE effects on the structure and thickness of eggshells
of many bird species. Particularly if the primary effect of DDE is on the
organic crystallization matrices, a 'disruption' if any of an endocrine
function could be a secondary effect. Moreover, virtually any metabolic
function is related one way or another to an endocrine activity. In this
context therefore, the use of the term 'endocrine disruption' in the absence
of any definitive demonstration of the cause(s) of eggshell thinning and
structural abnormalities would not appear to be justified.

10) The number of young bald eagles fledged per breeding pair in the
Great Lakes and along rivers supporting runs of anadromous fish increased
from 0.23 in 1977 to 0.87 in 1993 (Bowerman 1993). A goal of 1.0 young fledged/occupied
nest has been established by the Northern States Bald Eagle Recovery Plan
(Grier et al. 1983). This recovery is remarkable, particularly to those
of us who were bird-watching on the shores of the Great Lakes in the 1950s
and who followed the later population declines of bald eagles with dismay
and alarm. Smolen and Colborn, however, look at the remaining 13% of the
unfilled glass and predict catastrophe.

It is not therefore necessary to evoke a hypothesis that new, even more
insidious, chemicals with "hidden" effects will threaten the future
survival of the national emblem. The low production of young eagles in Florida
beginning in 1947, the continuing lower production on the shores of the
Great Lakes, and the absence of any natural reproduction in the marine environment
of southern California can all be considered as 'old' effects. Until DDE
contamination drops further in the Great Lakes, depression of bald eagle
reproduction will continue. As long as the Institute for Wildlife Studies
is able to continue its program in southern California, the bald eagle population
will be maintained­and continue to fly free in the Channel Islands­until
the DDE contamination finally clears. Meanwhile, the defective eggshells
will continue to provide a living example of an unpredictable deleterious
effect of an environmental contaminant.

Each of the other 'new' effects cited by Smolen and Colborn deserves
a comparable, detailed comment for which there is no space in this issue
of the Endangered Species UPDATE. Certainly, something happened to the sexuality
of the alligators of Lake Apopka in Florida; was this, however, an 'early
warning' of a new universal environmental threat or a unique, local event?
A possibility that the effects were local only comes from a recent report
(Semenza et al. 1997) that the nematicide DBCP had been manufactured at
a nearby pesticide manufacturing facility. Like the dieldrin and related
biocides from a factory on the Rhine that killed seabirds along the Netherlands
coast, and like DDT in factory wastes in Los Angeles and Alabama that grossly
contaminated local environments, DBCP from factory waste could have entered
the waters of Lake Apopka. This pesticide was banned in the US when it was
found to cause sterility among male workers in California (unused supplies
were then sent, shamefully, to Costa Rica). Hopefully, experiments to resolve
this question are currently underway.

Smolen and Colborn mention the "feminization and de-masculinization
of male birds", referring to a study by Ian Nisbet and his colleagues
of common terns of a colony in New Bedford Harbor that is highly contaminated
by PCBs (Nisbet et al. 1996). The "feminization" refers to the
appearance of female-type cells in the testes of male embryos. Not mentioned
is that the degree of feminization could not be correlated with the concentrations
of contaminants, and that so far at least it has been reported only in embryos;
whether or not the phenomenon in this colony is related to contaminants
is yet to be demonstrated. For the layman it is reasonable to believe that
"reproductivity and survivorship are compromised" in this population
of terns, but a scientist can hardly make such a statement in the absence
of any supporting information. The production of young is high, and the
colony has survived many years of high contamination.

Documentation of the existence of feminized adult male common terns,
or of any other species of birds for which "feminization" has
been claimed, would be the critical first step in the establishment of credibility.

The argument for simplified technologies with fewer, or no, synthetic
chemicals has its own, defensible, rationale. It is not, however, the same
argument that prompted the DDT hearings in Madison thirty years ago, - that
persistent, mobile, bioaccumulating and biologically active chemicals such
as DDT and the PCBs have no place in the longer-term technology. This technology
does have room for any combination of synthetic chemicals that does not
threaten either human health or wildlife. The public interest requires that
all participants in the continuing debates about synthetic chemicals distinguish
between these two separate and distinct arguments.

The chemical analysis of environmental samples, however, continues to
detect unidentified contaminants of undetermined significance. Chromatograms
frequently contain many more peaks representing unidentified organic contaminants
than peaks that have been identified in previous programs. Older chemists
remember the first electron capture chromatograms in the 1960s with the
unidentified peaks that turned out to be the PCBs. Vigilance to protect
both wildlife and human health from any unanticipated effect of chemical
technologies is required now more than ever. But the most significant of
the "new threats" to wildlife proposed by Smolen and Colborn are
already a half-century old and should not be confused with unanticipated
effects of newer chemicals.

Serious and important issues therefore remain. The argument, for example,
that genetic defects alone can not account for the abnormalities in the
Florida panther population, and that one or more contaminants might be involved,
deserves to be expanded. Meanwhile, however, in the absence of supporting
data, the central thesis of Smolen and Colborn-that many wildlife species,
including populations of endangered species, are now threatened by new 'hidden'
factors-lacks credibility.

Acknowledgments

Studies of the structure of bald eagle eggshells by scanning electron
microscopy were supported by the U.S. Fish & Wildlife Service and the
Bodega Bay Institute.

Broley, C.E. 1958. The plight of the American bald eagle.
Audubon Magazine 60:162-163;171.

Carson, R. 1962. Silent Spring. Houghton Mifflin Co., Boston.

Garcelon, D.K., R.W. Risebrough, W.M. Jarman, A.B. Chartrand,
and E.E. Littrell. 1989. Accumulation of DDE by bald eagles Haliaeetus
leucocephalus reintroduced to Santa Catalina Island in southern California.
Pages 491-494 in B.-U. Meyburg and R.D. Chancellor, eds. Raptors in the
Modern World. World Working Group on Birds of Prey and Owls. Berlin, London
and Paris.